Loss of centrosome integrity induces p38-p53-p21-dependent G1-S arrest

Nature Cell Biology

Volumn 9, Issue 2, 2007, Pages 160-170

  Mikule, Keith ^a,b   Delaval, Benedicte ^a   Kaldis, Philipp ^c   Jurcyzk, Agata ^a   Hergert, Polla ^d   Doxsey, Stephen ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b ArQule Biomedical Institute   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d WADSWORTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; CYCLIN DEPENDENT KINASE 2; PROTEIN P21; PROTEIN P53; SYNAPTOPHYSIN;

ANEUPLOIDY; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL DISRUPTION; CELL FUNCTION; CELL STRUCTURE; CENTROSOME; CONTROLLED STUDY; CYTOKINESIS; DIPLOIDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOSIS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

CELL LINE; CELLS, CULTURED; CENTROSOME; CYCLIN A; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASE INHIBITOR P21; G1 PHASE; HELA CELLS; HUMANS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; S PHASE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 33947270830     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1529     Document Type: Article

References (49)

1. Doxsey, S., Zimmerman, W. & Mikule, K. Centrosome control of the cell cycle. Trends Cell Biol. 15, 303-311 (2005).
2. Hinchcliffe, E. H. & Sluder, G. "It takes two to tango": Understanding how centrosome duplication is regulated throughout the cell cycle. Genes Dev. 15, 1167-1181 (2001).
3. Lacey, K. R., Jackson, P. K. & Steams, T. Cyclin-dependent kinase control of centrosome duplication. Proc. Natl Acad. Sci. USA 96, 2817-2822 (1999).
4. Pihan, G. A. et al. Centrosome defects and genetic instability in malignant tumors. Cancer Res. 58, 3974-3985 (1998).
5. Nigg, E. A. Centrosome aberrations: Cause or consequence of cancer progression? Nature Rev. Cancer 2, 815-825 (2002).
6. Khodjakov, A. & Rieder, C. L. Centrosomes enhance the fidelity of cytokinesis in vertebrates and are required for cell cycle progression. J. Cell Biol. 153, 237-242 (2001).
7. Hinchcliffe, E. H., Miller, F. J., Cham, M., Khodjakov, A. & Sluder, G. Requirement of a centrosomal activity for cell cycle progression through G1 into S phase. Science 291, 1547-1550 (2001).
8. Gromley, A. et al. A novel human protein of the maternal centriole is required for the final stages of cytokinesis and entry into S phase. J. Cell Biol. 161, 535-545 (2003).
9. Wong, C. & Stearns, T. Mammalian cells lack checkpoints for tetraploidy, aberrant centrosome number, and cytokinesis failure. BMC Cell Biol. 6, 6 (2005).
10. Uetake, Y. & Sluder, G. Cell cycle progression after cleavage failure: mammalian somatic cells do not possess a "tetraploidy checkpoint". J. Cell Biol. 165, 609-615 (2004).
11. Matsumoto, Y. & Mailer, J. L. A centrosomal localization signal in cyclin E required for Cdk2-independent S phase entry. Science 306, 885-888 (2004).
12. Gerdes, J. et al. Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J. Immunol. 133, 1710-1715 (1984).
13. Delgehyr, N., Sillibourne, J. & Bornens, M. Microtubule nucleation and anchoring at the centrosome are independent processes linked by ninein function. J. Cell Sci. 118, 1565-1575 (2005).
14. Casenghi, M. et al. Polo-like kinase 1 regulates NIp, a centrosome protein involved in microtubule nucleation. Dev. Cell 5, 113-125 (2003).
15. Gillingham, A. K. & Munro, S. The PACT domain, a conserved centrosomal targeting motif in the coiled-coil proteins AKAP450 and pericentrin. EMBO Rep. 1, 524-529 (2000).
16. Balczon, R., Simerly, C., Takahashi, D. & Schatten, G. Arrest of cell cycle progression during first interphase in murine zygotes microinjected with anti-PCM-1 antibodies. Cell Motil. Cytoskeleton 52, 183-192 (2002).
17. Gromley, A. et al. Centriolin anchoring of exocyst and SNARE complexes at the midbody is required for secretory-vesicle-mediated abscission. Cell 123, 75-87 (2005).
18. Nose, A. & Takeichi, M. A novel cadherin cell adhesion molecule: Its expression patterns associated with implantation and organogenesis of mouse embryos. J. Cell Biol. 103, 2649-2658 (1986).
19. Sherr, C. J. & Roberts, J. M. CDK inhibitors: Positive and negative regulators of G1-phase progression. Genes Dev. 13, 1501-1512 (1999).
20. La Terra, S. et al. The de novo centriole assembly pathway in HeLa cells: Cell cycle progression and centriole assembly/maturation. J. Cell Biol. 168, 713-722 (2005).
21. Kirkham, M., Muller-Reichert, T., Oegema, K., Grill, S. & Hyman, A. A. SAS-4 is a C. elegans centriolar protein that controls centrosome size. Cell 112, 575-587 (2003).
22. Leidel, S. & Gonczy, P. SAS-4 is essential for centrosome duplication in C. elegans and is recruited to daughter centrioles once per cell cycle. Dev. Cell 4, 431-439 (2003).
23. Habedanck, R., Stierhof, Y. D., Wilkinson, C. J. & Nigg, E. A. The Polo kinase Plk4 functions in centriole duplication. Nature Cell Biol. 7, 1140-1146 (2005).
24. Salisbury, J. L., Suino, K. M., Busby, R. & Springett, M. Centrin-2 is required for centriole duplication in mammalian cells. Curr. Biol. 12, 1287-1292 (2002).
25. Bettencourt-Dias, M., et al. SAK/PLK4 is required for centriole duplication and flagella development. Curr. Biol. 15, 2199-2207 (2005).
26. Balczon, R. et al. Dissociation of centrosome replication events from cycles of DNA synthesis and mitotic division in hydroxyurea-arrested Chinese hamster ovary cells. J. Cell Biol. 130, 105-115 (1995).
27. Jurczyk, A. et al. Pericentrin forms a complex with intraflagellar transport proteins and polycystin-2 and is required for primary cilia assembly. J. Cell Biol. 166, 637-643 (2004).
28. Pazour, G. J. & Witman, G. B. The vertebrate primary cilium is a sensory organelle. Curr. Opin. Cell Biol. 15, 105-110 (2003).
29. Rubbi, C. P. & Milner, J. Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J. 22, 6068-6077 (2003).
30. Zhan, Q., Carrier, F. & Fornace, A. J., Jr. Induction of cellular p53 activity by DNA-damaging agents and growth arrest. Mol. Cell Biol. 13, 4242-4250 (1993).
31. Wang, B., Matsuoka, S., Carpenter, P. B. & Elledge, S. J. 53BP1, a mediator of the DNA damage checkpoint. Science 298, 1435-1438 (2002).
32. Wu, G. S. The functional interactions between the p53 and MAPK signaling pathways. Cancer Biol. Ther. 3, 156-161 (2004).
33. Yee, A. S. et al. The HBP1 transcriptional repressor and the p38 MAP kinase: Unlikely partners in G1 regulation and tumor suppression. Gene 336, 1-13 (2004).
34. Kishi, H. et al. Osmotic shock induces G1 arrest through p53 phosphorylation at Ser33 by activated p38MAPK without phosphorylation at Ser15 and Ser20. J. Biol. Chem. 276, 39115-39122 (2001).
35. Lee, J. C. et al. A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 372, 739-746 (1994).
36. Harper, J. W., Adami, G. R., Wei, N., Keyomarsi, K. & Elledge, S. J. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75, 805-816 (1993).
37. el-Deiry, W. S. et al. WAF1, a potential mediator of p53 tumor suppression. Cell 75, 817-825 (1993).
38. Dutcher, S. K. Elucidation of basal body and centriole functions in Chlamydomonas reinhardtii. Traffic 4, 443-451 (2003).
39. Srsen, V., Gnadt, N., Dammermann, A. & Merdes, A. Inhibition of centrosome protein assembly leads to p53-dependent exit from the cell cycle. J. Cell Biol. 174, 625-630 (2006).
40. Leidel, S., Delattre, M., Cerutti, L., Baumer, K. & Gonczy, P. SAS-6 defines a protein family required for centrosome duplication in C. elegans and in human cells. Nature Cell Biol. 7, 115-125 (2005).
41. Pihan, G. A. et al. Centrosome defects can account for cellular and genetic changes that characterize prostate cancer progression. Cancer Res. 61, 2212-2219 (2001).
42. Grieshaber, S. S., Grieshaber, N. A., Miller, N. & Hackstadt, T. Chlamydia trachomatis causes centrosomal defects resulting in chromosomal segregation abnormalities. Traffic 7, 940-949 (2006).
43. Ploubidou, A. et al. Vaccinia virus infection disrupts microtubule organization and centrosome function. EMBO J. 19, 3932-3944 (2000).
44. Jouvenet, N. & Wileman, T. African swine fever virus infection disrupts centrosome assembly and function. J. Gen. Virol. 86, 589-594 (2005).
45. Vidair, C. A., Doxsey, S. J. & Dewey, W. C. Thermotolerant cells possess an enhanced capacity to repair heat-induced alterations to centrosome structure and function. J. Cell. Physiol. 163, 194-203 (1995).
46. Tuffanelli, D. L., McKeon, F., Kleinsmith, D. M., Burnham, T. K. & Kirschner, M. Anticentromere and anticentriole antibodies in the scleroderma spectrum. Arch. Dermatol. 119, 560-566 (1983).
47. Berthet, C., Aleem, E., Coppola, V., Tessarollo, L. & Kaldis, P. Cdk2 knockout mice are viable. Curr. Biol. 13, 1775-1785 (2003).
48. Morales, C. P. et al. Absence of cancer-associated changes in human fibroblasts immortalized with telomerase. Nature Genet. 21, 115-118 (1999).
49. Kennedy, B. K., Barbie, D. A., Classon, M., Dyson, N. & Harlow, E. Nuclear organization of DNA replication in primary mammalian cells. Genes Dev. 14, 2855-2868 (2000).